Macroconsumers are more important than specialist ... - Springer Link

Hydrobiologia (2010) 638:55–66 DOI 10.1007/s10750-009-0009-1

PRIMARY RESEARCH PAPER

Macroconsumers are more important than specialist macroinvertebrate shredders in leaf processing in urban forest streams of Rio de Janeiro, Brazil Timothy P. Moulton • Sandra A. P. Magalha˜es-Fraga Ernesto Fuentes Brito • Francisco A. Barbosa

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Received: 28 October 2008 / Revised: 7 November 2009 / Accepted: 23 November 2009 / Published online: 13 December 2009 Ó Springer Science+Business Media B.V. 2009

Abstract Coarse particulate organic matter is often broken down by specialist shredder invertebrates in temperate streams. In some tropical streams, larger, non-specialist, omnivorous fauna, (macroconsumers), particularly decapod shrimps and crabs, have been found to process coarse particulate matter. Larger shrimps and fish may also prey on or inhibit smaller invertebrates. Depending on the relative importance of larger and smaller fauna in leaf processing and in predatory interactions, we could expect that exclusion of larger fauna could either result in a decrease in leaf processing (if they were important in shredding or bioturbation) or increase in leaf processing if they

Handling editor: B. Oertli T. P. Moulton (&) E. F. Brito Departamento de Ecologia, IBRAG, Universidade do Estado do Rio de Janeiro, Rua Saõ Francisco Xavier, 524, Rio de Janeiro, RJ 20550-013, Brazil e-mail: [email protected] S. A. P. Magalha˜es-Fraga Nućleo de Gestaõ em Biodiversidade e Sau´de , Instituto de Tecnologia em Fa´rmacos, Fundaçaõ Oswaldo Cruz, Rio de Janeiro, RJ, Brazil e-mail: [email protected] F. A. Barbosa Departamento de Biologia Geral, Instituto de Cieˆncias Biolo´gicas, Universidade Federal de Minas Gerais, Av. Antonio Carlos, 6627, Belo Horizonte, MG 30161-970, Brazil e-mail: [email protected]

negatively affected smaller shredders. We tested this by excluding fauna of different sizes from leaf peaks using bags with different sizes of mesh –0.2 mm (exclusion of most fauna), 2 mm (exclusion of larger fauna), and 10 mm (access to most fauna). Bag effect on leaf processing was minimized by constructing the bags of the same, fine, material, and sewing a relatively small window of the required mesh size. The experiment was conducted on two occasions in three streams of the urban forest of Parque Estadual da Pedra Branca, city of Rio de Janeiro. The three streams differed in larger fauna of shrimps (Macrobrachium potiuna), crabs, tadpoles, and fish. Packs were incubated for six time intervals and the rate of leaf processing calculated as the exponential rate of loss of leaf material. Rate of leaf processing was faster in bags with the largest mesh size; the rates in the other two mesh sizes were not statistically different. Rates varied between experiments and among streams. We could not attribute the faster leaf processing to any particular component of the larger fauna; the patterns of differences among streams and between experiments were not associated with particular taxa. There was no general trend of fewer smaller fauna in the presence of macroconsumers; the few smaller taxa that were different between mesh sizes were variously less and more abundant in the 10mm mesh bags compared to the 2-mm. Known shredders were rare in the smaller fauna; the mining chironomid Stenochironomus was common, but was apparently not affected by larger fauna and apparently

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did not increase leaf processing. We conclude that macroconsumers and not smaller fauna had a positive effect on leaf processing, and this confirms a pattern observed in some other coastal Neotropical streams. Keywords Shredders Macrofauna Macroinvertebrates Decomposition Exclusion experiment Macrobrachium potiuna Crabs Tadpoles Fish Atlantic forest Introduction The effects of macroinvertebrates on the rate of leaf breakdown in aquatic systems have been shown to be important in many systems (Wallace & Webster, 1996). Various authors have commented on the apparent scarcity or lack of specialist shredding macroinvertebrates in tropical streams (Jacobsen et al., 2008)—in Hong Kong (Dudgeon & Wu, 1999; Li & Dudgeon, 2009), Kenya (Dobson et al., 2002), and Brazil (Ribas et al., 2006; Wantzen & Wagner, 2006; Gonçalves et al., 2006, 2007; Wantzen et al., 2008), but not in Australia (Cheshire et al., 2005) and high-altitude streams of Malaysia (Yule et al., 2009). Landeiro et al. (2008) found active trichopteran shredders in upland Amazonian streams. There have been some suggestions that litter processing by larger omnivores, such as the crustaceans Xiphocaris and Macrobrachium, can compensate for the lack of a specialist shredding guild of smaller macroinvertebrate in tropical streams (Crowl et al., 2001; March et al., 2001). In shredder-poor New Zealand streams, Usio (2000) found that omnivorous crayfish increased the rate of leaf processing and masked the potential effects of smaller insect shredders. On the other hand, predaceous and omnivorous fauna have been shown to have negative effects on smaller macroinvertebrates, which may have consequences at the basal resource level—a trophic cascade of the detrital food chain (Obernborfer et al., 1984; Konishi et al., 2001; Ruetz et al., 2002; Usio & Townsend, 2002; Greig & McIntosh, 2006). Rosemond et al. (2001) found that fishes and shrimps reduced the abundance of both macroinvertebrate detritivores and leaf detritus in streams in Costa Rica. In Amazonian upland streams, Landeiro et al. (2008) found that shrimps reduced the density of nonshredding chironomids, but did not affect the density of shredding trichopterans and mining chironomids. In

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Hydrobiologia (2010) 638:55–66

a stream in coastal forest of Rio de Janeiro the shrimp Macrobrachium olfersi inhibited baetid mayflies which in turn were important grazers of periphyton (Silveira & Moulton, 2000; Moulton et al., 2004). The negative effects of predators and omnivores are not restricted to consumption of prey—studies have shown that prey can be inhibited from feeding by the presence of putative predators (as with fish in Konishi et al., 2001 and with Macrobrachium in Moulton et al., 2004). We set up an experiment to investigate the effects of differently sized fauna on the rate of leaf processing using bags with different-sized meshes to exclude different sizes of fauna. We had opposing reasons for expecting that differently sized fauna might cause different effects. Macrobrachium shrimps occur in our streams, along with other larger omnivorous fauna which potentially increase leaf processing, either in concert with smaller macroinvertebrates or in substitution of smaller macroinvertebrates. On the other hand, the larger fauna might reduce or inhibit smaller fauna by interference or predation, as mentioned above. If this smaller fauna contained active leaf processing species the overall effect of larger fauna would be to diminish the rate of leaf processing, as with trout and an obligate trichopteran shredder (Greig & McIntosh, 2006) and fish and shredders (Ruetz et al., 2002). We studied streams of a large urban forest. These streams were depauperate in fish and shrimp species, but previous research had shown that they had a rich fauna of smaller macroinvertebrates (Moulton & Magalha˜es, 2003). The three streams that we studied had different larger fauna, and we expected that this might cause differences in leaf processing rate and effects on the smaller macroinvertebrates.

Methods Study site Our study sites were in Parque Estadual da Pedra Branca, a state park with full conservation status situated within the city of Rio de Janeiro (238520 to 238040 S and 438230 to 438320 W.). The park is arguably the largest totally urban forest in the world; its area is *125 km2 and the highest peak is 1,024 m in altitude. The climate is hot and humid, (Ko¨ppen Af) with little


or no hydric deficit. Annual rainfall is 1,215 mm and average for the driest month, August, is 60 mm. Much of the vegetation is secondary forest that regenerated from the original forest; there are patches of banana and other plantations and some human habitation in the park. We chose three third-order streams in neighboring catchments, Rio Engenho Novo, Rio Grande, and Rio Pequeno. The streams had wellembedded rocky substrate and sandy areas. The channels were well defined but not deeply incised. We chose slow-flowing sandy stretches with obvious organic-matter build-up for the placement of the experimental substrates. The park boundary is defined as the 100-m contour; the sites were immediately upstream from the boundary. The catchment above each stream is in reasonably good state of preservation, with high forest cover and intact riparian vegetation, but less than km below the sites, housing and slums impact the streams with sewage discharge, loss of riparian vegetation, and increased surface run-off. All streams discharge into coastal lagoons, but the sites are cut off for migratory species by heavy down-stream urban impact. Thus, the catadromous shrimp fauna of Macrobrachium (Decapoda: Palaemonidae) and Potimirim (Decapoda: Atyidae) species are not present and certain fish species have probably been lost. One non-catadromous shrimp, Macrobrachium potiuna, occurred in Rio Engenho Novo. Details of this phenomenon and its repercussions for conservation are found in Moulton et al. (2007). Other large fauna were: fish (Astyanax sp.—Characiformes: Characidae, Trichomycterus sp.—Siluriformes: Trichomycteridae, Poecilia reticulata—Cyprinodontiformes: Poeciliidae), crabs (Trichodactylus sp.— Decapoda: Trichodactylidae), and tadpoles (Bufo sp.—Anura: Bufonidae; Hyla albofrenata, Hylodes nasus, Phasmahyla guttata—Anura: Hylidae). The three streams had different proportions of these fauna: Rio Engenho Novo had the active predatory fish Astyanax sp. and the shrimp Macrobrachium potiuna; Rio Grande had the benthic-feeding catfish Trichomycterus sp., and Rio Grande and Rio Pequeno had many tadpoles and crabs. We term the fauna that were excluded by the 2-mm mesh ‘‘macroconsumers’’ (sensu Pringle & Hamazaki, 1998; Rosemond et al., 1998, 2001). In certain cases (notably the crabs and shrimps), small individuals of this fauna entered the 2-mm mesh exclusion, but the majority of the individuals were excluded. On the

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other hand, certain fauna not normally associated with the label macroconsumer might have been excluded from the 2-mm mesh bags. Notable in this category were the known shredding caddisflies Triplectides sp. (Leptoceridae) and Phylloicus sp. (Calamoceratidae) which have cases that potentially would not fit through 2 mm. However, we had observed these taxa to be rare in previous studies (Magalha˜es, 1998). The fauna that passed through the 2-mm mesh we term ‘‘smaller macroinvertebrates’’.

Leaf processing We selected the plant species Myrcia rostrata (Myrtaceae), an understorey tree with simple, oval, and medium-hard leaves approximately 2.5 9 6.5 cm. We constructed packs of 5 g of oven-dried leaves which were sewn together at one point and sewn into a nylon bag (15 9 20 cm). The bags were made from 0.2 mm nylon mesh and at their mouth we sewed a circular wire frame of circumference 30 cm with another mesh of 0.2, 2, or 10 mm. The different mesh sizes excluded differently sized aquatic animals: 0.2 mm excluded virtually all macroinvertebrates, 2 mm permitted the entrance of most macroinvertebrates (aquatic insects, smaller crustaceans, mites, and molluscs, etc.), 10 mm permitted the entrance of these and larger crustaceans (Macrobrachium and crabs), fish and tadpoles. Approximately 90% of the surface area of all bags was of the same material, 0.2 mm mesh. The bags were positioned in the stream so that their mouths with the different mesh sizes faced downstream. In this way, we minimized differences in water currents among bags of different treatments and minimized accumulation of particles inside bags. Such factors have been shown to cause artefacts in exclusion experiments using bags (Dangles et al., 2001). The bags were tied in lines of six of each mesh size on nylon cord, which was then anchored to a brick at each site. There were three sites in each of the three streams and the experiment was conducted twice (Experiment I from 13 October to 30 November 1999 and Experiment II from10 March to 14 April 2000) at the same sites. One bag of each mesh treatment was sampled from each site after regular intervals of immersion (2, 4, 8, 12, 24, and 48 days in the first experiment and 2, 4, 8, 16, 32, and 64 days in

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the second experiment). We measured the mass of the leaf pack before and after immersion. After retrieving the bags, the leaf pack was carefully removed, washed gently and adhering organisms were picked off under stereo microscope and preserved in 80% EtOH. The leaves were then dried to constant mass at 60°C and weighed. We considered only the material of the leaf pack; any extraneous organic material that remained in the bag was collected and weighed, but not considered part of the remaining leaf mass. We tested the relationship of dry mass to ash free dry mass on a subsample (30 packs) of the leaf packs and found that it did not vary with treatment, (AFDM/ DM = 0.947 ± 0.00254, mean ± standard error). Therefore, we did not incorporate this correction in our analysis and we present the measurement of leaf mass as dry mass. A complete account of the method and the design of the experiments is described in Magalha˜es-Fraga (2002); water chemistry and other details are in Magalha˜es et al. (2002). The rate of leaf processing was calculated from the linear regression of the natural log of the proportion of the remaining mass against the time of immersion (Gessner, 1991; Benfield, 1996). This analysis implies that the initial interval is discounted; it often represents a ‘‘leaching’’ phase of more rapid mass loss. The rate of mass loss in the subsequent intervals is assumed constant, conforming to the equation: Mt ¼ M0 ekt Mt loge ¼ kt M0 where Mt and M0 are the leaf mass at times 0 and t (days), e is the base of Napierian logarithms and k is the instantaneous rate of leaf mass loss per day. We compared processing rates among streams and mesh-size treatments and between experiments in an analysis of covariance of loge(Mt/M0) with Experiment (two levels), Stream (three streams) and Mesh size (three mesh sizes) as fixed factors and Time of immersion as the covariable. The interactions between the fixed factors and time of immersion provide the tests of different leaf processing rate associated with these factors (Quinn & Keough, 2002). The main effects of the analysis and their interactions are of no biological interest. We used the General Linear Model of SYSTAT (version 10, Systat Software, San Jose´, CA) for the analysis.

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We sorted the smaller macroinvertebrates under a stereo microscope (409) and identified them to different taxonomic levels. Larger fauna (fish, crustaceans, and tadpoles) were classified to species, as were molluscs. Chironomidae (Diptera) were not discriminated apart from the mining species Stenochironomus sp. Other insects were sorted to genus. Other groups were sorted to order. We tested the effect of mesh size on the abundance of macroinvertebrates using Repeated Measures ANOVA of factors Stream (three levels), Mesh treatment (two levels), and time of immersion as the repeated measure. Because of lost samples and the variability in abundance of the different taxa, the maximum number of repeated measures (six sampling days) was not always possible, and the separate analyses for each taxon and each experiment were run with the best possible design. We analyzed the most abundant taxa of the smaller macroinvertebrates that were expected to be able to traverse the 2-mm mesh. Results The streams were somewhat different from each other in terms of physical and chemical factors (Table 1); Rio Grande had a distinctly lower conductivity and the experimental sites of Rio Pequeno had the fastest stream flow. Rainfall was higher in Experiment I (125 mm during the course of the experiment, with a 24-h maximum of 26.5 mm); Experiment II had 65 mm total and 16.2 mm daily maximum. By normal patterns of rainfall in Rio de Janeiro we expected more rain in Experiment II, March–May, and the streams showed signs of much lower than normal discharge. Stream velocity was lower in Experiment II compared to Experiment I. Leaf processing The loss of leaf mass showed an initial sharp decrease, due presumably to leaching of labile material (Fig. 1). This was followed by an interval of stable or increased mass due, possibly, to colonization of microorganisms (=biofilm). After 8 days the leaf processing rate appeared linear, and we applied the analyses of leaf processing rate to the data from day 8 onwards. The rates of leaf processing (k *


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Table 1 Physical and chemical characteristics of the three streams in the two experiments Stream

Experiment

Velocity (m/s)

Temperature (8C)

Conductivity (lS/cm)

pH

Oxygen (mg/l)

Turbidity (NTU)

Engenho Novo

I

0.08

20.0

97.2

6.4

6.91

1.2

II

0.04

22.9

92.9

6.7

7.02

1.0

Grande

I

0.08

20.6

69.1

6.2

6.95

1.4

II

0.04

23.0

66.5

6.6

7.19

0.7

I

0.16

20.6

94.5

6.0

7.13

1.3

II

0.08

23.4

85.3

6.4

7.23

0.9

Pequeno

Seven measurements of each parameter were taken in each stream during each of the experiments

Fig. 1 Loss of leaf mass with time in three mesh-size treatments. The slope of the line is the instantaneous rate of leaf processing, k. Bars are standard error about the mean of three sites in three streams (n = 9)

0.003–0.019 day-1, Fig. 2) were similar to those found for Myrcia guyanensis and faster than the rates for several other species (Moretti et al., 2007). Leaf processing rate was significantly faster in the 10-mm mesh-size treatment, compared to the other treatments, as shown by the interaction of mesh-size

Fig. 2 Rate of leaf processing in three mesh-size treatments in three streams. Same legend as in Fig. 1. Bars are standard error (n = 3)

treatment and time (Table 2), by the slopes of the treatments in Fig. 1, and the k values in Fig. 2. Leaf processing rate was significantly slower in the second

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Table 2 Analysis of covariance of proportion of leaf mass remaining (loge) with respect to Experiment, Stream and Mesh treatments (fixed factors), and Time of immersion (covariable) Source

Sum of squares

df

Mean squares

Experiment

0.284

1

0.284

Stream

0.033

2

0.016

Mesh

0.030

2

0.015

Time

4.545

1

4.545

Stream * Experiment

0.151

2

0.075

Mesh * Experiment Mesh * Stream

0.250 0.009

2 4

0.125 0.002

F-ratio

Experiment * Time

0.281

1

0.281

59***

Stream * Time

0.087

2

0.044

9.2***

Mesh * Time

0.475

2

0.237

50***

Mesh * Stream * Time

0.020

4

0.005

1.04

Error

0.900

190

0.005

The interactions between fixed factors and Time determine if the rate of leaf processing was significant with respect to those factors. The main effects and interactions between fixed factors are not biologically interesting. *** P \ 0.001

experiment (Table 2; Fig. 2), and varied among streams. There was not, however, a significant difference in the mesh-size effect among streams, judged by the lack of significance of the Mesh * Stream * Time interaction (Table 2), although the difference between mesh treatments appeared smallest in Rio Pequeno in the second experiment (Fig. 1). Fauna Almost 19,000 individuals of smaller macroinvertebrates were counted in 201 samples; they were distributed in the following higher taxa: Chironomidae (72%), Other Diptera (0.28%), Ephemeroptera (12%), Plecoptera (0), Odonata (1.2%), Trichoptera (0.85%), Hemiptera (0.10%), Coleoptera (2.3%), Collembola (0.27%), Acari (3.48%), Copepoda (2.4%), Ostracoda (1.2%), Hirudinea (0.04%), Oligochaeta (0.63%), Nematoda (0.12%), and Mollusca (2.3%). The smaller macroinvertebrates varied considerably among the three streams and between experiments (Table 3). The mining chironomid, Stenochironomus, and other chironomids were abundant, reaching levels of 100 individuals per leaf pack and showed similar patterns of colonization among streams, although different

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patterns between experiments. The abundance of other chironomids did not vary with mesh size; Stenochironomus was more abundant in the largemesh bags in Experiment I (Table 3). Amongst the Ephemeroptera, Cloeodes was more common in the 2-mm mesh treatment than the 10-mm in Experiment I, but not in Experiment II (Table 3). Baetodes showed the opposite trend and was more common in 10 mm mesh than 2 mm in Experiment I. Miroculis and Caenis were more common in Rio Engenho Novo. No trichopteran taxa were sufficiently common for individual analysis. The known shredder trichopterans Phylloicus and Triplectides were present in 16 and 5% of the samples at densities of 0.36 and 0.11 individuals per leaf pack, respectively. Triplectides was not found in samples from Rio Grande and Rio Pequeno and Phylloicus was very rare in these streams. Both species were found in bags of both mesh sizes. The macroconsumers were generally restricted to the larger mesh, as required by the experimental design, but small crabs (Trichodactylus) entered the small-mesh bags in Experiment I. Macrobrachium shrimps were common in Rio Engenho Novo. Tadpoles were common in Rio Grande and Rio Pequeno in Experiment I, but less so in Experiment II. The species varied between streams, with Hyla albofrenata and Bufo sp. in Rio Grande and Hylodes nasus and Phasmohyla guttata in Rio Pequeno. The catfish, Trichomycterus, was found only in Rio Grande. The introduced guppy, Poecilia reticulata, occurred in Rio Grande and Rio Pequeno. The characine, Astyanax sp., was commonly observed in Rio Engenho Novo, but not in the other streams. It was seen entering the bags, but was not captured in the samples.

Discussion The rate of leaf processing was greater in the 10-mm mesh bags than in those of the other two mesh sizes. Macroconsumers excluded by 2 mm mesh apparently increased the rate of leaf processing. Leaf processing was not significantly different between the 2-mm and the 0.2-mm mesh bags. This implied that smaller macroinvertebrates that passed through 2 mm mesh


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Table 3 Repeated measures ANOVA of most abundant taxa Taxon

Source

Experiment I Repeated measures (days)

Experiment II P value

Comparison of means

Repeated measures (days)

P value Comparison of means

Stenochironomus (Diptera: Chironomidae) 8, 16, 24, 48

32, 64

Stream

0.002 EN [ RP = RG

0.031 EN [ RP = RG

Mesh

0.047 L [ S

0.141

Stream * Mesh

0.118

0.875

Other Chironomidae 2, 4, 8, 16, 32, 64

2, 4, 16, 32, 64

Stream

0.186

0.004 RP [ RG = EN

Mesh Stream * Mesh

0.261 0.089

0.69 0.608

Cloeodes (Ephemeroptera: Baetidae) 2, 4, 8, 16, 24 Stream

2, 4, 16, 32, 64 \0.001 RP [[EN [ RG

0.272 \0.001 S [ L

Mesh Stream * Mesh

0.456

0.518

0.563

Baetodes (Ephemeroptera: Baetidae) 2, 4, 8, 16, 24, 48 Stream

2, 4, 16, 32 0.901

0.08

\0.001 L [ S 0.418

Mesh Stream * Mesh

RP [ RG = EN

0.819 0.695

Leptohyphes (Ephemeroptera: Leptohyphidae) 2, 4, 8, 16, 24, 48

2, 4, 16, 32, 64

Stream

0.074 RP = RG [ EN

Mesh

0.293

\0.001 RP [ RG [ EN 0.989

Stream * Mesh

0.266

0.139

Miroculis (Ephemeroptera: Leptophlebiidae) 2, 4, 8, 16, 24, 48 Stream Mesh

16, 32, 64 \0.001 EN [[RG [ RP 0.171 (L [ S)

\0.001 EN [ RG [ RP 0.561

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Table 3 continued Taxon

Source

Experiment I Repeated measures (days)

Experiment II P value

Stream * Mesh

Comparison of means

Repeated measures (days)

0.347

P value Comparison of means 0.905

Caenis (Ephemeroptera: Caenidae) 2, 4, 8, 16, 24

2, 16, 32 \0.001 EN [ RP = RG

Stream

\0.001 EN [ RP = RG

Mesh

0.762

0.306

Stream * Mesh

0.479

0.734

Acari 2, 4, 8, 16, 24, 48

2, 4, 16, 32

Stream

0.119 (RG [ RP [ EN)

0.024 EN [ RG = RP

Mesh

0.002 S [ L

0.001 S [ L

Stream * Mesh

0.375

0.195

Copepoda 2, 4, 8, 16, 24, 48

2, 4, 16, 32, 64 (RP [ RG [ EN)

\0.001 EN [ RG = RP

Stream

0,177

Mesh

0,818

0.368

Stream * Mesh

0,727

0.051

Heterelmis (Elmidae: Coleoptera) 2, 4, 8, 16, 24, 48

2, 4, 16, 32, 64

Stream

0.275

0.167

Mesh

0.775

0.931

Stream * Mesh

0.477

0.306

The repeated measures (days of immersion) available for analysis varied among taxa due to varying abundance and lost samples. Comparison of means was not formally tested, but estimated from graphs of least squared means Stream codes: EN Rio Engenho Novo; RG Rio Grande; RP Rio Pequeno Mesh codes: S = 2 mm; L = 10 mm

did not affect the rate of leaf processing compared to the rate without this fauna. This result was potentially an artefact of the experimental method: bags with the largest mesh could intrinsically have had a higher leaf processing rate than bags with the two smaller meshes. This would probably have been caused by greater water movement within the large-mesh bags and a greater potential for material to exit through the larger mesh. We safeguarded against this with the design of the bags: only the mouth of the bag was of the different

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mesh size, the remaining 90% of the bag material was the same, 0.2 mm mesh material in all of the bags. We aligned the bags with the mouth facing downstream so that the bags presented the same, fine, mesh to the oncoming current. We did not include any loose or accumulated material in the weighing of the material remaining after immersion, and thus circumvented one of the criticisms of Dangles et al. (2001). If, indeed, the mesh size had affected the leaf processing rate, it would have done so in a particular manner in which 10 mm mesh increased the rate


compared to the 0.2-mm mesh while 2 mm mesh did not. We think this unlikely, and we think it more likely that the experimental design truly tested for differences related to differently sized fauna. We are also confident that the leaf packs inside bags were able to be colonized by the available fauna. Obviously, the conditions inside the bags were different in some respects to those of leaves freely exposed to the stream. Water flow would have been slowed and presumably the bags could have been preferentially colonized by fauna that preferred slower current and enclosed conditions. In a previous experiment, Magalha˜es (1998) compared leaf processing and associated fauna in leaf packs within open and closed bags and without bags. Macroinvertebrates were generally more abundant in the leaf packs of open bags compared to bagless packs. Rate of leaf processing was, however, higher in bagless packs, which apparently indicated that water movement in bagless packs affected leaf processing more than biotic factors. On the other hand, water movement and biotic fragmentation may interact positively, and in the present study the reduced water movement within bags could have reduced biotic-mediated leaf processing. However, it was important for the comparison of the different faunas that the water movement be as similar as possible among mesh treatments, and we are confident that the relative rates of leaf processing between treatments were realistic. We could not identify which part of the larger fauna was responsible for the effect. There was no obvious difference in leaf processing among streams such that we could associate differences with the different faunas of different streams. On the contrary, our evidence leads us to postulate that several elements of the larger fauna are responsible for the results, since no likely candidate was common in all three streams (Fig. 2). The larger crustaceans, crabs (Trichodactylus), and shrimps (Macrobrachium), have been shown to be important shredders in other studies (Usio, 2000; Crowl et al., 2001; March et al., 2001; Rosemond et al., 2001; Dobson et al., 2002). Tadpoles are generally not considered to be shredders; they usually rasp surfaces to feed on soft material and biofilm (Ranvestel et al., 2004). They possibly cause loss of leaf material by their activities. The fish species encountered in this study are considered predaceous, and although it is unlikely that they assimilate detrital organic matter, they

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possibly cause leaf material to be lost by their feeding activities. Some other taxa were more common in the larger mesh bags at least in some streams at one time, but they were unlikely contributors to the observed difference in leaf processing, e.g., the mayflies Baetodes and Miroculis. The lack of difference in leaf processing rate between the 2 and 0.2-mm mesh-size treatments implies that smaller macroinvertebrates were not important in this process. The mining chironomid, Stenochironomus, was common in the 2 and 10-mm mesh-size treatments, and reached densities of 100 individuals per leaf pack in all streams of the first experiment. It was absent in the 0.2-mm treatment, but it apparently did not increase the rate of leaf processing (see also Moulton & Magalha˜es, 2003). The other common taxa of mayflies and other groups also apparently did not increase leaf processing. The known shredding taxa of trichopterans, Triplectides, and Phylloicus were rare in Rio Engenho Novo and virtually absent in the other streams. They occurred in both 2 and 10 mm mesh bags. The result adds to evidence of the lack or scarcity of shredders and invertebrate decomposers in many tropical streams (Dudgeon & Wu, 1999; Dobson et al., 2002; Mathuriau & Chauvet, 2002; Ribas et al., 2006; Wantzen & Wagner, 2006, Gonçalves et al., 2006, 2007; Wantzen et al., 2008; Li & Dudgeon, 2009). Shredding taxa have been recorded in many surveys of Brazilian streams (Oliveira et al., 1999; Crisci-Bispo et al., 2007; Nessimian et al., 2008). Further experimental studies of processing rates are necessary before we can generalize about the importance of these shredders in leaf processing, but we can note that the present study confirms other Brazilian studies which found no significant involvement of macroinvertebrates in leaf processing (Ribas et al., 2006; Wantzen & Wagner, 2006; Gonçalves et al., 2007). On the other hand, we did not observe many cases that could be interpreted as a negative effect of macroconsumers on smaller macroinvertebrates, as might have been expected from the results of other studies (Obernborfer et al., 1984; Usio, 2000; Rosemond et al., 2001; Konishi et al., 2001; Usio & Townsend, 2002; Ruetz et al., 2002; Greig & McIntosh, 2006). One possible case was that of the baetid mayfly Cloeodes, which was significantly less abundant in bags with large-mesh size (Table 3). This species was seen to have a negative interaction

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with Macrobrachium in a stream in Rio de Janeiro (Silveira & Moulton, 2000; Moulton et al., 2004) and possibly showed this behavior in Rio Engenho Novo in the present study and perhaps avoided other macroconsumers in the other two streams. In contrast, another baetid mayfly, Baetodes, was more common in the larger mesh bags (Table 3) in Experiment I, and we find it difficult to argue strongly for a predator effect in one case and the opposite in the other case of genera from the same family. Chironomidae were shown to be heavily preyed upon by shrimp by Rosemond et al. (2001), March et al. (2001), and Landeiro et al. (2008); their sedentary habit and general lack of protection often make them prey to larger organisms (Armitage, 1995). On the other hand Souza et al. (2007) concluded that chironomids reacted more strongly to trophic resources and habitat than to predation in a study which excluded shrimps and mayflies. The present study showed no difference in the abundance of ‘‘other chironomids’’ in bags of different mesh size, which implies that macroconsumers did not affect their abundance. The mining chironomid, Stenochironomus, appeared more abundant in the presence of macrofauna in Experiment I. Apart from mites, the taxa did not show effects that were attributable to predation by larger fauna. We conclude that in our urban forest streams, there was little effect of larger fauna on smaller fauna and little potential for an associated trophic cascade. We may speculate about what limits the fauna in their feeding on the leaves of this experiment and whether this represents a general tendency for tropical streams (Dobson et al., 2002; Moulton, 2006; Boulton et al., 2008; Lau et al., 2009). It would appear that leaves were little utilized directly by fauna. The recognized shredders were scarce and the results imply that no other small macroinvertebrates processed leaves to any detectable degree. The mining chironomid, Stenochironomus, was common, but at least within the limits of this experiment it did not increase the rate of leaf processing. The macroconsumers apparently increased the loss of leaf material, but we may question if they utilized leaf material as food, or if they merely increased its rate of loss through bioturbation or ingestion of non-assimilated material. We have no data on carbon flow through the food chain of the particular streams of this experiment, but if we can extrapolate from the results of Brito et al. (2006) in a

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similar but not urban stream, we can suppose that the fish and shrimps did not assimilate much allochthonous plant carbon. Results from other tropical streams also showed that the shrimps assimilated carbon of algal origin rather than that of allochthonous plant material (March & Pringle, 2003; Lau et al., 2009). Acknowledgments This research was carried out by SAPM-F as part of a doctoral program at Universidade Federal de Minas Gerais; we thank Conselho Nacional de Pesquisas (CNPq) for the scholarship. The research forms part of Projeto Integrado 520549/97 0, CNPq, of TPM. We thank the many students who helped with field work and discussions. Several reviewers considerably improved this article.

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